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Articles, Behavioral/Cognitive

Optogenetic Manipulation of Activity and Temporally Controlled Cell-Specific Ablation Reveal a Role for MCH Neurons in Sleep/Wake Regulation

Tomomi Tsunematsu, Takafumi Ueno, Sawako Tabuchi, Ayumu Inutsuka, Kenji F. Tanaka, Hidetoshi Hasuwa, Thomas S. Kilduff, Akira Terao and Akihiro Yamanaka
Journal of Neuroscience 14 May 2014, 34 (20) 6896-6909; https://doi.org/10.1523/JNEUROSCI.5344-13.2014
Tomomi Tsunematsu
1Department of Neuroscience II, Research Institute of Environmental Medicine, Nagoya University, Nagoya 464-8601, Japan,
2The Japan Society for the Promotion of Sciences, Tokyo 102-8472, Japan,
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Takafumi Ueno
3Laboratory of Biochemistry, Department of Biomedical Sciences, Graduate School of Veterinary Medicine, Hokkaido University, Sapporo 060-0818, Japan,
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Sawako Tabuchi
1Department of Neuroscience II, Research Institute of Environmental Medicine, Nagoya University, Nagoya 464-8601, Japan,
2The Japan Society for the Promotion of Sciences, Tokyo 102-8472, Japan,
4Department of Physiological Sciences, The Graduate University for Advanced Studies, Okazaki 444-8787, Japan,
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Ayumu Inutsuka
1Department of Neuroscience II, Research Institute of Environmental Medicine, Nagoya University, Nagoya 464-8601, Japan,
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Kenji F. Tanaka
5Department of Neuropsychiatry, School of Medicine, Keio University, Tokyo 160-8582, Japan,
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Hidetoshi Hasuwa
6Research Institute for Microbial Disease, Osaka University, Suita 565-0781 Japan, and
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Thomas S. Kilduff
7Center for Neuroscience, Biosciences Division, SRI International, Menlo Park, California 94025
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Akira Terao
3Laboratory of Biochemistry, Department of Biomedical Sciences, Graduate School of Veterinary Medicine, Hokkaido University, Sapporo 060-0818, Japan,
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Akihiro Yamanaka
1Department of Neuroscience II, Research Institute of Environmental Medicine, Nagoya University, Nagoya 464-8601, Japan,
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Abstract

Melanin-concentrating hormone (MCH) is a neuropeptide produced in neurons sparsely distributed in the lateral hypothalamic area. Recent studies have reported that MCH neurons are active during rapid eye movement (REM) sleep, but their physiological role in the regulation of sleep/wakefulness is not fully understood. To determine the physiological role of MCH neurons, newly developed transgenic mouse strains that enable manipulation of the activity and fate of MCH neurons in vivo were generated using the recently developed knockin-mediated enhanced gene expression by improved tetracycline-controlled gene induction system. The activity of these cells was controlled by optogenetics by expressing channelrhodopsin2 (E123T/T159C) or archaerhodopsin-T in MCH neurons. Acute optogenetic activation of MCH neurons at 10 Hz induced transitions from non-REM (NREM) to REM sleep and increased REM sleep time in conjunction with decreased NREM sleep. Activation of MCH neurons while mice were in NREM sleep induced REM sleep, but activation during wakefulness was ineffective. Acute optogenetic silencing of MCH neurons using archaerhodopsin-T had no effect on any vigilance states. Temporally controlled ablation of MCH neurons by cell-specific expression of diphtheria toxin A increased wakefulness and decreased NREM sleep duration without affecting REM sleep. Together, these results indicate that acute activation of MCH neurons is sufficient, but not necessary, to trigger the transition from NREM to REM sleep and that MCH neurons also play a role in the initiation and maintenance of NREM sleep.

  • ablation
  • cell fate
  • channelrhodopsin2
  • hypothalamus
  • optogenetics
  • REM sleep

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The Journal of Neuroscience: 34 (20)
Journal of Neuroscience
Vol. 34, Issue 20
14 May 2014
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Optogenetic Manipulation of Activity and Temporally Controlled Cell-Specific Ablation Reveal a Role for MCH Neurons in Sleep/Wake Regulation
Tomomi Tsunematsu, Takafumi Ueno, Sawako Tabuchi, Ayumu Inutsuka, Kenji F. Tanaka, Hidetoshi Hasuwa, Thomas S. Kilduff, Akira Terao, Akihiro Yamanaka
Journal of Neuroscience 14 May 2014, 34 (20) 6896-6909; DOI: 10.1523/JNEUROSCI.5344-13.2014

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Optogenetic Manipulation of Activity and Temporally Controlled Cell-Specific Ablation Reveal a Role for MCH Neurons in Sleep/Wake Regulation
Tomomi Tsunematsu, Takafumi Ueno, Sawako Tabuchi, Ayumu Inutsuka, Kenji F. Tanaka, Hidetoshi Hasuwa, Thomas S. Kilduff, Akira Terao, Akihiro Yamanaka
Journal of Neuroscience 14 May 2014, 34 (20) 6896-6909; DOI: 10.1523/JNEUROSCI.5344-13.2014
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Keywords

  • ablation
  • cell fate
  • channelrhodopsin2
  • hypothalamus
  • optogenetics
  • REM sleep

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